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Programmed cell death or desiccation tolerance: two possible routes for wheat endosperm cells

Published online by Cambridge University Press:  22 February 2007

Elena A. Golovina ,
Folkert A. Hoekstra  and
Adriaan C. van Aelst
Elena A. Golovina*
Affiliation:
Timiryazev Institute of Plant Physiology, Botanicheskaya 35, Moscow, 127276, Russia Laboratory of Plant Physiology, Department of Plant Sciences, Wageningen University, Arboretumlaan 4, 6703 BD Wageningen, The Netherlands
Folkert A. Hoekstra
Affiliation:
Laboratory of Plant Physiology, Department of Plant Sciences, Wageningen University, Arboretumlaan 4, 6703 BD Wageningen, The Netherlands
Adriaan C. van Aelst
Affiliation:
Laboratory of Experimental Plant Morphology and Cell Biology, Department of Plant Sciences, Wageningen University, Arboretumlaan 4, 6703 BD Wageningen, The Netherlands
*
*Correspondence Fax: +31-317-484740 Email: [email protected]
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Abstract

The fate of cells in the endosperm of developing wheat kernels was investigated under normal conditions and upon premature slow drying on the cut ear. To follow the changes in membrane integrity and cellular ultrastructure, an electron spin resonance (ESR) spin probe technique and low temperature scanning electron microscopy (LTSEM) were used. ESR data indicated that during development, the relative amount of cells with intact membranes decreased and became almost zero at the stage of mass maturity, i.e. several days before the onset of maturation drying. This suggests that the death of starchy endosperm cells is a developmental phenomenon rather than one induced by water loss. Even at 8 days after anthesis (daa), early in the differentiation phase, a considerable proportion of endosperm cells had already lost plasma membrane integrity. Comparison of ESR data with LTSEM micrographs revealed that the loss of plasma membrane integrity occurred early in the starch accumulation process, from which it was concluded that the programmes of starch accumulation and developmental death are simultaneously switched on. When the differentiation into starchy endosperm was arrested by premature slow drying of kernels on the cut ear, meristematic cells (aleurone initials) acquired desiccation tolerance as assessed by the combination of the spin probe technique and LTSEM. In contrast, fast drying caused immediate death of these cells. Thus, meristematic endosperm cells have the competence to acquire desiccation tolerance. This occurs upon premature slow drying or during normal differentiation into aleurone cells, but is lost when the cells differentiate into starchy endosperm.

Keywords

Desiccation tolerancedevelopmentendospermprogrammed cell deathstarch accumulationTriticum aestivum
Type
Research Article
Information
Seed Science Research , Volume 10 , Issue 3 , September 2000 , pp. 365 - 379
Copyright
Copyright © Cambridge University Press 2000

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References

Barlow, E.W.R., Lee, J.W., Munns, R. and Smart, M.G. (1980) Water relations of the developing wheat grain. Australian Journal of Plant Physiology 7, 519–525.Google Scholar
Batygina, T.B. (1987) The grain of cereals. Leningrad, Nauka Publishers.Google Scholar
Bennett, M.D., Rao, M.K., Smith, J.B. and Baylis, M.W. (1973) Cell development in the anther, the ovule and the young seed of Triticum aestivum L. var. Chinese Spring. Philosophical Transactions of the Royal Society of London Series B Biological Sciences 266, 39–81.Google Scholar
Berg, S.P. and Nesbitt, D.M. (1979) Chromium oxalate: a new spin label broadening agent for use with thylakoids. Biochimica et Biophysica Acta 548, 608–615.CrossRefGoogle ScholarPubMed
Berger, F. (1999) Endosperm development. Current Opinion in Plant Biology 2, 28–32.CrossRefGoogle ScholarPubMed
Berliner, L.J. (1976) Spin labeling: theory and applications. New York, Academic Press.Google Scholar
Bethke, P.C., Lonsdale, J.E., Fath, A. and Jones, R.L. (1999) Hormonally regulated programmed cell death in barley aleurone cells. The Plant Cell 11, 1033–1045.CrossRefGoogle ScholarPubMed
Brenchley, W.E. (1909) On the strength and development of the grain of wheat (Triticum vulgare). Annals of Botany 23, 117–139.CrossRefGoogle Scholar
Brunori, A. (1967) Relationship between DNA synthesis and water content during ripening of Vicia faba seeds. Caryologia 20, 333–338.CrossRefGoogle Scholar
Buckner, B., Janick-Buckner, D., Gray, J. and Johal, G.S. (1998) Cell-death mechanisms in maize. Trends in Plant Science 3, 218–223.CrossRefGoogle Scholar
Buttrose, M.S. (1963) Ultrastructure of the developing wheat endosperm. Australian Journal of Biological Sciences 16, 305–317.CrossRefGoogle Scholar
Colombo, L., Franken, J., Van der Krol, A.R., Wittich, P.E., Dons, H.J.M. and Angenent, G.C. (1997) Downregulation of ovule-specific MADS box genes from petunia results in maternally controlled defects in seed development. The Plant Cell 9, 703–715.Google ScholarPubMed
DeMason, D.A. (1997) Endosperm structure and development. pp. 73–116in Larkins, B.A.; Vasil, I.K. (Eds) Advances in cellular and molecular biology in plants. Vol. 4. Cellular and molecular biology of plant seed development. Dordrecht, the Netherlands, Kluwer Academic Publishers.CrossRefGoogle Scholar
Eaton, S.S. and Eaton, G.R. (1978) Interaction of spin labels with transition metals. Coordination Chemistry Reviews 26, 451–453.CrossRefGoogle Scholar
Evers, A.D. (1970) Development of the endosperm of wheat. Annals of Botany 34, 547–555.CrossRefGoogle Scholar
Friedman, W.E. (1992) Evidence of a pre-angiosperm origin of endosperm: implication for the evolution of flowering plants. Science 255, 336–339.CrossRefGoogle ScholarPubMed
Friedman, W.E. (1995) Organismal duplication, inclusive fitness theory and altruism: understanding the evolution of endosperm and the angiosperm reproductive syndrome. Proceedings of the National Academy of Sciences USA 92, 3913–3917.CrossRefGoogle ScholarPubMed
Golovina, E.A., Hoekstra, F.A. and Hemminga, M.A. (1998) Drying increases intracellular partitioning of amphiphilic substances into the lipid phase: Impact on membrane permeability and significance for desiccation tolerance. Plant Physiology 118, 975–986.CrossRefGoogle ScholarPubMed
Golovina, E.A., Tikhonov, A.N. and Hoekstra, F.A. (1997) An electron paramagnetic resonance spin probe study of membrane permeability changes with seed aging. Plant Physiology 114, 383–389.CrossRefGoogle ScholarPubMed
Keith, A.D. and Snipes, W. (1974) Viscosity of cellular protoplasm. Science 183, 666–668.CrossRefGoogle ScholarPubMed
Kuo, A., Cappelluti, S., Cervantes-Cervantes, M., Rodriguez, M. and Bush, D.S. (1996) Okadaic acid, a protein phosphate inhibitor, blocks calcium changes, gene expression and cell death induced by gibberellin in wheat aleurone cells. The Plant Cell 8, 259–269.Google Scholar
Lopes, M.A. and Larkins, B.A. (1993) Endosperm origin, development, and function. The Plant Cell 5, 1383–1399.Google Scholar
Mares, D.J., Norstog, K. and Stone, B.A. (1975) Early stages in the development of wheat endosperm. I. The changes from free nuclear to cellular endosperm. Australian Journal of Botany 23, 311–326.CrossRefGoogle Scholar
Mares, D.J., Stone, B.A., Jeffrey, C. and Norstog, K. (1977) Early stages in the development of wheat endosperm. 2. Ultrastructural observations on cell wall formation. Australian Journal of Botany 25, 599–613.CrossRefGoogle Scholar
Marsden, M.P.F. and Meinke, D.W. (1985) Abnormal development of the suspensor in an embryo-lethal mutant of Arabidopsis thaliana. American Journal of Botany 72, 1801–1812.CrossRefGoogle Scholar
Morrison, I.N., Kuo, J. and O'Brien, T.P. (1975) Histochemistry and fine structure of developing wheat aleurone cells. Planta 123, 105–116.CrossRefGoogle ScholarPubMed
Morrison, I.N. and O'Brien, T.P. (1976) Cytokinesis in the developing wheat grain; division with and without a phragmoplast. Planta 139, 57–67.CrossRefGoogle Scholar
Morrison, W.R. (1978) Cereal lipids. pp. 221–348in Pomeranz, Y. (Ed.) Advances in cereal science and technology. Vol. II. St. Paul, MN, American Association of Cereal Chemists.Google Scholar
Morse II, P.D. (1977) Use of the spin label tempamine for measuring the internal viscosity of red blood cells. Biochemical and Biophysical Research Communications 77, 1486–1491.CrossRefGoogle Scholar
Olsen, O.-A., Linnestad, C. and Nichols, S.E. (1999) Developmental biology of the cereal endosperm. Trends in Plant Science 4, 253–257.CrossRefGoogle ScholarPubMed
Olsen, O.-A., Potter, R.H. and Kalla, R. (1992) Histodifferentiation and molecular biology of developing cereal endosperm. Seed Science Research 2, 117–131.CrossRefGoogle Scholar
Percival, J. (1921) The wheat plant. London, Duckworth and Co.Google Scholar
Rogers, S.O. and Quatrano, R.S. (1983) Morphological staging of wheat caryopsis development. American Journal of Botany 70, 308–311.CrossRefGoogle Scholar
Schwartz, B.W., Yeung, E.C. and Meinke, D.W. (1994) Disruption of morphogenesis and transformation of the suspensor in abnormal suspensor mutants of Arabidopsis. Development 120, 3235–3245.CrossRefGoogle ScholarPubMed
Simmonds, D.H. and O'Brien, T.P. (1981) Morphological and biochemical development of the wheat endosperm. pp. 5–70in Pomeranz, Y. (Ed.) Advances in cereal science and technology. Vol. IV. St. Paul, MN, American Association of Cereal Chemists.Google Scholar
Wang, M., Oppedijk, B.J., Lu, X., Van Duijn, B. and Schilperoort, R.A. (1996) Apoptosis in barley aleurone during germination and its inhibition by abscisic acid. Plant Molecular Biology 32, 1125–1134.CrossRefGoogle ScholarPubMed
Yaklich, R.W., Wergin, W.P. and Erbe, E.F. (1994) Use of low temperature scanning electron microscopy to observe frozen hydrated seed tissues of Glycine max. Seed Science Research 4, 347–353.CrossRefGoogle Scholar
Yaklich, R.W., Wergin, W.P. and Erbe, E.F. (1996) Use of low temperature SEM to locate free water in frozen, hydrated seed tissues of Glycine max (Leguminosae). American Journal of Botany 83, 550–555.CrossRefGoogle Scholar
Young, T.E., Gallie, D.R. and DeMason, D.A. (1997) Ethylene-mediated programmed cell death during maize endosperm development of wild-type and shrunken2 genotypes. Plant Physiology 115, 737–751.CrossRefGoogle ScholarPubMed